Abstract
Objectives
Evaluation of the impact of a biscuit containing the probiotics Bifidobacterium longum Bar33 and Lactobacillus helveticus Barl3 on the intestinal microbiota in the elderly.
Design
Randomized double-blind placebo-controlled trial.
Participants
Thirty-two elderly volunteers living in Italy. The group was composed of 19 women and 13 men aged between 71 and 88 years (mean 76).
Intervention
Subjects were randomized in two groups consuming one dose of the probiotics-containing biscuit or placebo once a day for 30 days.
Measurements
For each subject the intestinal microbiota was characterized using the phylogenetic microarray platform HTF-Microbi. Array before and after intervention.
Results
Our data demonstrated that one-month consumption of a probiotics-containing biscuit was effective in redressing some of the age-related dysbioses of the intestinal microbiota. In particular, the probiotic treatment reverted the age-related increase of the opportunistic pathogens Clostridium cluster XI, Clostridium difficile, Clostridium perfringens, Enterococcus faecium and the enteropathogenic genus Campylobacter.
Conclusion
The present study opens the way to the development of elderly-tailored probiotic-based functional foods to counteract the age-related dysbioses of the intestinal microbiota.
Similar content being viewed by others
References
Tumbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The human microbiome project. Nature 449:804–810.
Lee YK, Mazmanian SK (2010) Has the mlcrobiota played a critical role in the evolution of die adaptive immune system? Science 330:1768–1773.
O’Hara AM, Shanahan P (2006) The gut flora as a forgotten organ. BMBO Reports 7:688–693.
Hooper LV, Macpherson AJ (2010) Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 10:159–169.
Biagi E, Candela M, Pairweather-Tait S, Rranceschi C, Brigidi P (2012) Ageing of the human metaorganism: die microbial counterpart. Age 34:247–267.
Ostan R, Bucci L, Capri M, Salvioli S, Scurti M, Pini B, Monti D, Pranceschi P (2008) Immuno senescence and immu no genetics of human longevity. Neuroimmunomodulation 15:224–240.
Shanley DP, Aw D, Manley NR, Palmer DB (2009) An evolutionary perspective on the mechanisms of immuno senescence. Trends Immunol 30:374–381.
Hayashi H, Sakamoto M, Kitahara M, Benno Y (2003) Molecular analysis of fecal microbiota in elderly individuals using 16S rDNA library and T-RPLP. Microbiol Immunol 47:557–570.
Mueller S, Saunier K, Hanisch C, Norin E, Aim L, Midtvedt T, Cresci A, Silvi S, Orpianesi C, Verdenelli MC, Clavel T, Koebnick C, Zunft HIP, Doré J, Blaut M (2006) Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol 72:1027–1033.
Makivuokko H, Tiihonen K, Tynkkynen S, Paulin L, Rautonen N (2010) The effect of age and non-steroidal anti-inflammatory drugs on human intestinal microbiota composition. Br J Nutr 103:227–234.
Gavini P, Cayuela C, Antoine JM, Lecoq C, Le Pabure B, Membre JM, Neut C (2001) Differences in distribution of bifidobacteria! and enterobacterial species in human fecal microflora of three different (children, adults, elderly) age groups. Microb Ecol Health Dis 13:40–45.
Woodmansey EJ, McMurdo MET, Macfarlane CI, Macfarlane S (2004) Comparison of compositions and metabolic activities of fecal microbiotas in young adults and in antibiotic-treated and non-antibiotic treated elderly subjects. Appl Environ Microbiol 70:6113–6122.
Mariat D, Hrmesse O, Levenez P, Guimaraes VD, Sokol H, Dore J, Corthier G, Puret JP (2009) The Hrmicutes/Bacteroidetes ratio of die human microbiota changes with age. BMC Microbiol 9:123.
Rajilic-Stojanovic M, Heilig HG, Molenaar D, Kajander K, Surakka A, Smidt H, de Vos WM (2009) Development and application of the Human Intestinal Tract Chip, a phylogenetic micro array: analysis of die universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ Microbiol 11:1736–1751.
Simor AE, Bradley SP, Strausbaugh U, Crossley K, Nicolle LE (2002) Clostridium difficile in long-term-care facilities for the elderly. Infect Control Hosp Epidemiol 23:696–703.
Neish AS (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136:65–80.
Macia L, Thorburn AN, Binge LC, Marino E, Rogers KE, Maslowski KM, Vieira AT, Kranich J, Mackay CR (2012) Microbial influences on epithelial integrity and immune function as a basis for inflammatory diseases. Immunol Rev 245:164–176.
Cohen JE (2003) Human population: the next half century. Science 302:1172–1175.
Christensen K, Doblhammer G, Rau R, Vaupel JW (2009) Ageing populations: the challenges ahead. Lancet 374:1196–1208.
Hayflick L (2000) The future of aging. Nature 408:267–269.
Hebuterne X (2003) Gut changes attributed to ageing: effects on intestinal microflora. Curr Opin Clin Nutr Metab Care 6:49–54.
Tuohy KM (2007) Inulin-type fructans in healthy aging. J Nutr 137:2590S–2593S.
Tiihonen K, Ouwehand AC, Rautonen N (2010) Human intestinal microbiota and healthy ageing. Ageing Res Rev 9:107–116.
Björklund M, Ouwehand AC, Forssten SD, Nikkilä J, Tiihonen K, Rautonen N, Lahtinen SJ (2011) Gut microbiota of healthy elderly NSAID users is selectively modified with the administration of Lactobacillus acidophilus NCFM and lactitol. Age: DOI 10.1007/s 11357-011-9294-5.
Lahtinen SJ, Forssten S, Aakko J, Granlund L, Rautonen N, Salminen S, Viitanen M, Ouwehand AC (2012) Probiotic cheese containing Lactobacillus rhamnosus HN001 and Lactobacillus acidophilus NCFM(®) modifies subpopulations of fecal lactobacilli and Clostridium difficile in the elderly. Age 34:133–143.
Chiang BL, Sheih YH, Wang LH, Lial CH, Gills HS (2000) Enhancing immunity by dietary consumption of a probiotic lactic acid bacterium (Bifidobacterium lactis HN019): optimization and definition of cellular immune responses. Eur J Clin Nutr 54:849–855.
Arunachalam K, Gills HS, Chandra RK (2000) Enhancement of natural immune function by dietary consumption of Bifidobacterium lactis (HN019). Eur J Clin Nutr 54:263–267.
Gill HS, Rutherfurd KJ, Cross ML (2001a) Dietary probiotic supplementation enhances natural killer cells activity in the elderly: an investigation of age-related immunological changes. J Clin Immunol 21:264–271.
Gill HS, Rutherfurd KJ, Cross ML, Gopal PK (2001b) Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. Am J Clin Nutr 74:833–839.
Sheih YH, Chiang BL, Wang LH, Liao CK, Gills HS (2001) Systemic immunity enhancing effects in healthy subjects following dietary consumption of the lactic acid bacterium Lactobacillus rhamnosus HN001. J Am Coll Nutr 20:149–156.
Takeda K, Okumura K (2007) Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the human NK-cell activity. J Nutr 137:7913–793 S.
Amhed M, Prased J, Gill H, Stevenson L, Gopal P (2007) Impact of consumption of different levels of Bifidobacterium lactis HN019 on the intestinal microflora of elderly human subjects. J Nutr Health Aging 11:26–31.
Lahtinen SJ, Tammela L, Korpela J, Parhiala R, Ahokoski H, Mykkanen H, Salminen S (2009) Probiotics modulate the Bifidobacterium microbiota of elderly nursing home residents. Age 31:59–66.
Matsumoto M, Sakamoto M, Benno Y (2009) Dynamics of fecal microbiota in hospitalized elderly fed prebiotic LKM512 yogurt. Microbiol Immunol 53:421–432.
Candela M, Perna F, Carnevali P, Vitali B, Ciati R, Gionchetti P, Rizzello F, Campieri M, Brigidi P (2008) Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol 125:286–292.
Roselli M, Finamore A, Nuccitelli S, Carnevali P, Brigidi P, Vitali B, Nobili F, Rami R, Garaguso I, Mengheri E (2009) Prevention of TNBS-induced colitis by different Lactobacillus and Bifidobacterium strains is associated with an expansion of gammadeltaT and regulatory T cells of intestinal intraepithelial lymphocytes. Liflamm Bowel Dis 15:1526–1536.
Candela M, Consolandi C, Severgnini M, Biagi E, Castiglioni B, Vitali B, De Bellis G, Brigidi P (2010) High taxonomic level fingerprint of the human intestinal microbiota by ligase detection re action-universal array approach. BMC Microbiol 19:116.
Castiglioni B, Rizzi E, Frosini A, Sivonen K, Rajaniemi P, Rantala A, Mugnai MA, Ventura S, Wilmotte A, Boutte C, Grubisic S, Balthasart P, Consolandi C, Bordoni R, Mezzelani A, Battaglia C, De Bellis G (2004) Development of a universal microarray based on the ligation detection reaction and 16S rrna gene polymorphism to target diversity of cyanobacteria. Appl Environ Microbiol 70:7161–7172.
Rajilic-Stojanovic M, Smidt H, de Vos WM (2007) Diversity of the human gastrointestinal tract microbiota revisited. Environ Microbiol 9:2125–2136.
Tumbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI (2009) A core gut microbiome in obese and lean twins. Nature 457:480–484.
Mazmanian SK, Round JL, Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453:620–625.
Hamady M, Knight R (2009) Microbial community profiling for human microbiome projects: Tools, techniques, and challenges. Genome Res 19:1141–1152.
Consolandi C, Severgnini M, Castiglioni B, Bordoni R, Frosini A, Battaglia C, Rossi Bernardi L, De Bellis G (2006) A structured chitosan-based platform for biomolecule attachment to solid surfaces: application to DNA microarray preparation. Bioconjug Chem 17:371–377.
Leps J, Smilauer P (2003) Multivariate analysis of ecological data using CANOCO: Cambridge University Press, Cambridge.
Biagi E, Nylund L, Candela M, Bucci L, Ostan R, Nikkila J, Monti D, Satokari R, Franceschi C, Brigidi P, de Vos WM (2010) Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PloS One 5:el0667.
Png CW, Linden SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH (2010) Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 105:2420–2428.
Pedron T, Sansonetti P (2008) Commensals, bacterial pathogens and intestinal inflammation: an intriguing ménage à trois. Cell Host & Microbes 3:344–347.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rampelli, S., Candela, M., Severgnini, M. et al. A probiotics-containing biscuit modulates the intestinal microbiota in the elderly. J Nutr Health Aging 17, 166–172 (2013). https://doi.org/10.1007/s12603-012-0372-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12603-012-0372-x